Genetic analysis of juvenile (Oncorhynchus kisutch) off and Washington reveals few Columbia River wild fish

Item Type article

Authors Teel, David J.; Van Doornik, Donald M.; Kuligowski, David R.; Grant, W. Stewart

Download date 30/09/2021 19:04:38

Link to Item http://hdl.handle.net/1834/31006 640

Abstract—Little is known about the Genetic analysis of juvenile coho salmon ocean distributions of wild juvenile coho salmon off the Oregon-Washington (Oncorhynchus kisutch) off Oregon and coast. In this study we report tag recov- eries and genetic mixed-stock estimates Washington reveals few Columbia River wild fi sh* of juvenile fi sh caught in coastal waters near the Columbia River plume. To sup- David J. Teel port the genetic estimates, we report an allozyme-frequency baseline for 89 Donald M. Van Doornik wild and hatchery-reared coho salmon David R. Kuligowski spawning populations, extending from Conservation Biology Division northern California to southern Brit- Northwest Fisheries Science Center ish Columbia. The products of 59 allo- 2725 Montlake Boulevard East zyme-encoding loci were examined with Seattle, Washington 98112-2097 starch-gel electrophoresis. Of these, 56 Present address (for D. J. Teel): Manchester Research Laboratory loci were polymorphic, and 29 loci had 7305 Beach Drive E. P levels of polymorphism. Average 0.95 Port Orchard, Washington 98366 heterozygosities within populations Email address (for D. J. Teel): [email protected] ranged from 0.021 to 0.046 and aver- aged 0.033. Multidimensional scaling of chord genetic distances between sam- W. Stewart Grant ples resolved nine regional groups that were sufficiently distinct for genetic P.O. Box 240104 mixed-stock analysis. About 2.9% of the Anchorage, Alaska 99524-0104 total gene diversity was due to differ- ences among populations within these regions, and 2.6% was due to differences among the nine regions. This allele-fre- quency data base was used to estimate Nearshore and riverine distributions the fi rst to use genetic data to estimate the stock proportions of 730 juvenile coho salmon in offshore samples col- of maturing Pacifi c salmon (Oncorhyn- the stock origins of ocean mixtures of lected from central Oregon to northern chus spp.) are well known, largely juvenile coho salmon (O. kisutch). Washington in June and September- because of the prevalence of salmon One goal of our study was to cre- October 1998−2000. Genetic mixed- fi sheries and the tremendous amount ate a baseline of allelic frequencies in stock analysis, together with recoveries of information gathered to manage spawning populations of coho salmon of tagged or fi n-clipped fi sh, indicates these fi sheries. Out-migration timings throughout the Pacifi c Northwest and that about one half of the juveniles and abundances of smolts in streams California. These data were previously came from Columbia River hatcheries. as they migrate to the sea are also well used by the National Marine Fisheries Only 22% of the ocean-caught juveniles known, but information on the distribu- Service (NMFS) to defi ne evolutionarily were wild fi sh, originating largely from tions and stock origins of wild juveniles signifi cant units (ESUs) for evaluation coastal Oregon and Washington rivers (about 20%). Unlike previous studies in marine waters has been limited by under the Endangered Species Act of tagged juveniles, both tag recoveries two factors. The fi rst is that a large (Johnson et al., 1991; Weitkamp et al., and genetic estimates indicate the pres- amount of effort is needed to sample 1995). In the present study, we examine ence of fi sh from British Columbia and marine-phase juveniles, which gener- levels of variability among populations Puget Sound in southern waters. The ally occur at low densities (Godfrey, and use mixed-stock simulations to as- most salient feature of genetic mixed 1965; Hartt and Dell, 1986; Orsi et al., sess the usefulness of such a data set stock estimates was the paucity of wild 2000). The second factor is that stock as a baseline for genetic mixed-stock juveniles from natural populations in origins have been determined only for analysis. A second goal was to use this the Columbia River Basin. This result coded-wire−tagged (CWT) hatchery baseline of population data to estimate refl ects the large decrease in the abun- fi sh (e.g. Pearcy and Fisher, 1988; Orsi the stock compositions of juvenile coho dances of these populations in the last few decades. et al., 2000). Because only small propor- salmon collected in the early and late tions of hatchery juveniles are tagged, summers of 1998, 1999, and 2000 off samples of ocean-caught salmon are the Oregon and Washington coasts by largely a mixture of hatchery and wild the NMFS (Emmett and Brodeur, 2000). fi sh of unknown stock origins. Genetic We use a standard approach to genetic mixed-stock analysis, although used mixed-stock analysis that yields propor- routinely to estimate the stock compo- tional estimates of stock origin of fi sh sitions of mature returning salmon (e.g. in a mixed-stock sample (e.g., Pella and Manuscript approved for publication Milner et al., 1985; Shaklee et al., 1999; Milner, 1987). We compare early and 15 January 2003 by Scientifi c Editor. Beacham et al., 2001), has not been Manuscript received 4 April 2003 at fully exploited to estimate stock origins * Contribution 388 to the U.S. GLOBEC pro- NMFS Scientifi c Publications Offi ce. of immature salmon (but see Guthrie et gram, Woods Hole Oceanographic Institute, Fish. Bull. 101:640–652 (2003). al., 2000). The study we describe here is Woods Hole, MA 02543. Teel et al.: Genetic analysis of juvenile Oncorhynchus kisutch 641

late summer samples to detect seasonal shifts in stock 128° 124° 122°W compositions along the coast and make comparisons with 126° earlier tag-recovery studies to search for decadal shifts British Columbia in the marine distributions of particular stocks. Recent

efforts at Pacifi c Northwest hatcheries to mark the major-

r e

ity of their releases of coho salmon with a fi n clip provide v i

50N° R

new opportunities to estimate proportions of hatchery and r

e

88 s 89 a wild coho salmon in ocean samples (Beamish et al., 2000; r

F Lawson and Comstock, 2000). We therefore report genetic 86 87 85 estimates for hatchery-marked and unmarked fi sh in ocean 83 samples and use these estimates to identify hatchery and 84 82 63 75-81 wild population origins of ocean juvenile coho salmon. 73-74 La Push +++++ 59-62 64 57-58 65 70-72 66-68 69 Materials and methods +++++ +++++ 53-56 Location of +++++ 50-52 Washington To establish an allele-frequency baseline, populations of coastal pelagic 46° 34-37 38-39 coho salmon were sampled from 89 hatcheries, streams, trawl surveys +++++ 32-33 40-42 Columbia and rivers between 1984 and 1999 (Fig. 1, Table 1). Samples ++++ 31 43-49 River of skeletal muscle, eye, liver, and heart tissues were col- ++++ 30 lected from adults during spawning operations in hatcher- ++++ 26-29 ies or from whole juvenile fi sh in hatchery rearing ponds. 23-25 Cape Perpetua All hatchery broods sampled were the progeny of al least +++ 21-22 50 adult fi sh. Wild juveniles were sampled in natal streams 17-20 and rivers by electroshocking. Wild adult fi sh were sampled 11-16 Oregon in spawning areas by gaffi ng and dip-netting. 10 9 8 r ive Samples of juvenile coho salmon in marine waters were R 7 Rogue collected during NMFS coastal pelagic trawl surveys 42° (Emmett and Brodeur, 2000). Trawls consisted of one- 5 h r t Rive half-hour long surface tows with a 264 Nordic rope trawl a m a l along nine transects perpendicular to shore ranging from K La Push, Washington (47°55′N) to Cape Perpetua, Oregon 4 (44°15′N) (Fig. 1). Sampling stations began 1−5 nautical 6 California

miles offshore and continued, in about 5 nautical-mile

r

e v

(nmi) increments, to about 30 nmi offshore. Marine ju- i

R

veniles were sampled 16−24 June and 21−30 September o

t 3 n

1998, 16−24 June and 21 September−1 October 1999, and 2 e m

a

r

c 17−25 June and 19−24 September 2000. Fish were mea- a

N S sured and examined for the presence of fi n clips and coded 38° wire tags (CWTs). Juveniles in their fi rst ocean summer were separated from older coho salmon by length by using a modifi cation of the criteria of Pearcy and Fisher (1990). 1 Fish with fork lengths less than 330 mm (June) and 450 0 100 200 km mm (September–October) were considered to be juveniles in their fi rst year in the ocean. Fish with CWTs, and there- fore of known brood year, provided supporting evidence for Figure 1 these criteria with the assumption that growth of hatchery Locations of ocean sampling transect lines (+) and 89 coho salmon and wild fi sh was similar. populations in California, Oregon, Washington, and British Colum- bia. Numbers correspond to population names in Table 1. Tissue samples or whole juvenile fi sh were frozen on dry ice or in liquid nitrogen and stored at −80°C prior to electrophoretic analysis. We used the methods of Aeber- sold et al. (1987) for sample preparation and horizontal Genotypic frequencies of polymorphic loci for each base- starch-gel protein electrophoresis. Electrophoretic condi- line sample were examined for departures from expected tions for 30 enzymes, for which we obtained reliable and Hardy-Weinberg proportions with a Fisher’s exact test interpretable data for 59 loci, are reported in an appendix (Guo and Thompson, 1992) by using GENEPOP version that can be retrieved at the Northwest Fisheries Science 3.1 (Raymond and Rousset, 1995). Hardy-Weinberg tests Center website [http://www.nwfsc.noaa.gov]. Guidelines were performed on isoloci (comigrating protein products of by Utter et al. (1987) were used to infer genotypes from duplicated loci) following Waples (1988). banding patterns. Locus and allelic nomenclature follows We estimated allelic frequencies for each sample. Allelic Shaklee et al. (1990). frequencies for isoloci were calculated as mean frequen- 642 Fishery Bulletin 101(3)

Table 1 Sample information and indices of genetic variability for coho salmon from the Pacifi c Northwest and California. Map codes refer

to Figure 1. Indices of genetic variability are %P0.95 = percentage of P0.95 loci and H = heterozygosity.

Source Number of

Region and map code Year sampled fi sh %P0.95 H

California coast 1 Scott Creek 1994 21 12.5 0.039 2 Little River 1994 27 14.3 0.040 3 Warm Springs Hatchery 1994, 1994 160 16.1 0.041 4 Mad River Hatchery 1994 120 17.9 0.040 Klamath River to Cape Blanco 5 Iron Gate Hatchery 1994 120 9.0 0.021 6 Trinity Hatchery 1984, 1994 218 9.0 0.028 7 Rogue River (Illinois River, Greyback Creek) 1993 40 7.2 0.022 8 Cole Rivers Hatchery, stock no. 52 (Rogue River) 1993 100 9.0 0.030 9 North Fork Elk and Elk Rivers 1993 32 7.2 0.021 Oregon coast 10 Sixes River (Crystal and Edson Creeks) 1993 44 7.2 0.026 11 New River (Bether and Morton Creeks) 1993 62 10.7 0.034 12 Butte Falls Hatchery, stock no. 44 (Coquille River) 1993 100 9.0 0.036 13 Cole Rivers Hatchery, stock no. 37 (South Fork ) 1993 129 10.7 0.034 14 Coos River ( and Marlow Creek) 1993, 1997 50 12.5 0.033 15 Butte Falls Hatchery, Eel River stock no. 63 1993 100 7.2 0.032 16 Ten Mile Lake 1992 56 7.2 0.030 17 Rock Creek Hatchery, stock no. 55 (Umpqua River) 1993 100 7.2 0.029 18 North Umpqua River (Williams Creek) 1993, 1997 67 7.2 0.025 19 Butte Falls Hatchery, stock no. 18 (Umpqua River) 1993 100 7.2 0.027 20 Smith River (Halfway Creek) 1993 40 10.7 0.034 21 Fall Creek Hatchery, stock no. 113 (Tahkenitch River) 1993 100 7.2 0.030 22 Siuslaw River 1996 51 9.0 0.029 23 Fall Creek Hatchery, stock no. 31 (Alsea River) 1993 100 14.3 0.040 24 Fall Creek Hatchery, stock no. 43 (Alsea River) 1993 95 9.0 0.037 25 Alsea River 1996 62 10.7 0.031 26 Beaver Creek 1993 62 9.0 0.035 27 Yaquina River 1996 54 12.5 0.043 28 Salmon River Hatchery, stock no. 33 (Siletz River) 1993 100 12.5 0.041 29 Siletz River (Forth of July, Sunshine, and Buck Creeks) 1993 50 10.7 0.033 30 Salmon River Hatchery, stock no. 36 (Salmon River) 1993 100 10.7 0.037 31 Trask River Hatchery, stock no. 34 (Trask River) 1992, 1993 220 16.1 0.039 32 Nehalem River Hatchery, stock no. 99 (Nehalem River) 1992 80 12.5 0.045 33 Nehalem River Hatchery, stock no. 32 (Nehalem River) 1993 100 14.3 0.044 Columbia River 34 Lewis and Clark River 1991, 1993 36 12.5 0.038 35 Big Creek Hatchery 1991 80 12.5 0.040 36 Grays River Hatchery 1987, 1991 200 7.2 0.033 37 Clatskanie River (Carcus Creek) 1991, 1992, 1996 113 10.7 0.033 38 Cowlitz Hatchery early-run 1991 80 9.0 0.027 39 Cowlitz Hatchery late-run 1991, 1992 180 7.2 0.031 40 Scappoose River (Siercks, Raymond, and Milton Creeks) 1991 44 14.3 0.041 41 Lewis River Hatchery early-run 1991 80 5.4 0.027 42 Lewis River Hatchery late-run 1991 80 12.5 0.032 43 North Fork Clackamas River early-run 1998a 48 16.1 0.036 44 North Fork Clackamas River late-run 1999a 45 14.3 0.028 45 Eagle Creek Hatchery 1991, 1992 180 7.2 0.037 continued Teel et al.: Genetic analysis of juvenile Oncorhynchus kisutch 643

Table 1 (continued)

Source Number of

Region and map code Year sampled fi sh %P0.95 H

46 Sandy River Hatchery 1991, 1992 180 10.7 0.046 47 Sandy River 1991, 1992, 1996 124 10.7 0.043 48 Bonneville Hatchery 1991, 1992 180 10.7 0.043 49 Willard Hatchery 1991 80 7.2 0.032 South Washington coast 50 Naselle River Hatchery 1991 100 9.0 0.029 51 Nemah River Hatchery 1991 100 10.7 0.029 52 Willapa River Hatchery 1991 100 9.0 0.031 53 Chehalis River (Stillman Creek) 1995 71 9.0 0.026 54 Chehalis River (Satsop River, Bingham Creek) 1995 98 10.7 0.028 55 Bingham Creek Hatchery 1991,1 1992,1 1995 180 9.0 0.027 56 Chehalis River (Hope Creek) 1994, 1995, 1996 171 9.0 0.030 North Washington coast 57 Queets River 1995 99 9.0 0.028 58 Clearwater River 1995 100 7.2 0.029 59 Bogachiel River 1987 80 10.7 0.030 60 Sol Duc Hatchery Summer Run 19941 80 7.2 0.030 61 Sol Duc River Summer Run 1995 120 10.7 0.030 62 Sol Duc Hatchery Fall Run 19951 80 9.0 0.032 63 Hoko River 1987 96 9.0 0.033 Puget Sound and Hood Canal 64 Dungeness Hatchery 1987 80 12.5 0.037 65 Quilcene Hatchery 19941 100 9.0 0.025 66 North Fork Skokomish River 1994,1 19951 126 7.2 0.030 67 Dewatto River 1994,11995,1 19961 169 9.0 0.028 68 Minter Creek Hatchery 1992,1 19951 80 9.0 0.035 69 Soos Creek Hatchery 1994,1 1995, 1996 680 9.0 0.034 70 Snoqualmie River (Harris Creek) 1987 120 7.2 0.034 71 Snoqualmie River (Grizzly Creek) 1994,1 1995,1 19961 215 7.2 0.030 72 North Fork Skykomish River (Lewis Creek) 19951 102 9.0 0.032 73 North Fork Stillaguamish River (Fortson Creek) 1987, 1989 1 200 9.0 0.031 74 North Fork Stillaguamish River (Mcgovern Creek) 1987 40 10.7 0.032 75 Upper Skagit River 1993 127 9.0 0.033 76 Skagit River (Carpenter Creek) 1993 139 9.0 0.032 77 Skagit River (West Fork Nookachamps Creek) 1987, 1993 220 9.0 0.035 78 Skagit River (Baker River) 1992 1 303 10.7 0.036 79 Skagit River (Suiattle River, All Creek) 1987, 1993 200 10.7 0.032 80 Skagit River (Upper Sauk River) 1992, 1993 200 9.0 0.034 81 Skagit River (Upper Cascade River) 1992, 1993 224 9.0 0.031 82 Samish River (Ennis Creek) 1994, 1 1995, 1 1996 1 167 9.0 0.035 British Columbia 83 Chilliwack River Hatchery 1984 100 10.7 0.034 84 Cowichan River Hatchery 1984 80 9.0 0.036 85 Big Qualicum Hatchery 1989, 1 1991 180 10.7 0.037 86 Robertson Creek Hatchery 1984 100 9.0 0.030 87 Capilano Hatchery 1989, 1 1991 200 12.5 0.038 88 Squamish River Hatchery 19881 98 7.2 0.035 Upper Fraser River 89 Spius River Hatchery 1987 200 10.7 0.035 Mean 10.0 0.033

1 Sample taken from adult fi sh. All other samples were from juvenile fi sh. 644 Fishery Bulletin 101(3)

Table 2 Enzymes and study results for 59 loci in samples of 89 coho salmon populations from the Pacifi c Northwest and California.

Number of Range of Enzyme or Enzyme commission Locus populations common allele protein name number abbrev. polymorphic frequency

Aspartate aminotransferase 2.6.1.1 sAAT-1,2* 36 1.000−0.966 sAAT-3* 1 1.000−0.956 sAAT-4* 71 1.000−0.839 Adenosine deaminase 3.5.4.4 ADA-1* 34 1.000–0.924 ADA-2* 15 1.000–0.929 Aconitate hydratase 4.2.1.3 mAH-1* 2 1.000–0.992 mAH-2* 22 1.000–0.919 mAH-3* 3 1.000–0.944 sAH* 60 1.000–0.849 Adenylate kinase 2.7.4.3 AK* 4 1.000–0.993 Alanine aminotransferase 2.6.1.2 ALAT* 12 1.000–0.958 Creatine kinase 2.7.3.2 CK-A1* 8 1.000–0.971 CK-A2* 22 1.000–0.919 CK-C1* 4 1.000–0.983 CK-C2* 9 1.000–0.972 CK-B* 1 1.000–0.999 Esterase 3.1.-.- EST-1* 85 1.000–0.652 Fructose-bisphosphate aldolase 4.2.1.13 FBALD-3* 1 1.000–0.996 FBALD-4* 14 1.000–0.962 Formaldehyde dehydrogenase (glutathione) 1.2.1.1 FDHG* 33 1.000–0.954 Fumarate hydratase 4.2.1.2 FH* 43 1.000–0.835 b-N-Acetylgalactosaminidase 3.2.1.53 bGALA* 89 0.889–0.357 Glyceraldehyde-3-phosphate dehydrogenase 1.2.1.12 GAPDH-2* 64 1.000–0.713 GAPDH-3* 26 1.000–0.867 GAPDH-4* 9 1.000–0.975 GAPDH-5* 0 1.000–1.000 Glucose-6-phosphate isomerase 5.3.1.9 GPI-A* 17 1.000–0.906 GPI-B1* 1 1.000–0.962 GPI-B2* 47 1.000-0.815 Glutathione reductase 1.6.4.2 GR* 6 1.000–0.988 continued

cies over both loci and treated as a single tetrasomic locus. populations were depicted with multidimensional scaling Following the recommendations of Waples (1990), allelic (MDS, NTSYS-PC, Exeter Software, NY). Allele-frequency frequencies of samples taken in different years from the variation among baseline populations was partitioned same location were combined. In general, little temporal (Chakraborty et al., 1982) into two geographic levels: 1) allele-frequency variation was detected in coho salmon populations within regions; and 2) among regions (Table 1). populations sampled over years (Van Doornik et al., 2002; These regions were delimited by geography and by genetic present study). Levels and patterns of genetic variation groupings in the MDS analyses. within and between populations were estimated with 56 We used the maximum likelihood procedures of Pella and polymorphic loci (Table 2). Average expected heterozygos- Milner (1987) and the Statistical Package for Analyzing ity per locus (isoloci excluded) for each population was Mixtures (SPAM; Debevec et al., 2000) to estimate stock calculated by using an unbiased estimator (Nei, 1978). contributions to simulated and actual mixtures of coho

The proportion of P0.95 loci was computed for each popula- salmon. Estimates were made by using 56 polymorphic loci tion, in which a locus was considered to be polymorphic (Table 2) and 89 baseline populations, except for analysis if the frequency of the most common allele was ≤0.95. of marked (hatchery) fi sh where only hatchery populations Chord distances (Cavalli-Sforza and Edwards, 1967) were were used (Table 1). Allocations to individual baseline computed between all pairs of populations with BIOSYS populations were then summed to estimate contributions of (Swofford and Selander, 1981), and relationships among regional stock groups (Pella and Milner, 1987). Average mix- Teel et al.: Genetic analysis of juvenile Oncorhynchus kisutch 645

Table 2 (continued)

Number of Range of Enzyme or Enzyme commission Locus populations common allele protein name number abbrev. polymorphic frequency

Isocitrate dehydrogenase 1.1.1.42 mIDHP-1* 4 1.000–0.964 mIDHP-2* 11 1.000–0.799 sIDHP-1* 11 1.000–0.948 sIDHP-2* 29 1.000–0.851 Lactate dehydrogenase 1.1.1.27 LDH-A1* 7 1.000–0.700 LDH-A2* 2 1.000–0.995 LDH-B1* 18 1.000–0.942 LDH-B2* 20 1.000–0.956 LDH-C* 0 1.000–1.000 Malate dehydrogenase 1.1.1.37 sMDH-A1,2* 35 1.000–0.976 sMDH-B1,2* 21 1.000–0.947 Mannose-6-phosphate isomerase 5.3.1.8 MPI* 41 1.000–0.897 α-Mannosidase 3.2.1.24 MAN* 5 1.000–0.981 Dipeptidase 3.4.-.- PEPA* 63 1.000–0.895 Tripeptide amino peptidase 3.4.-.- PEPB-1* 10 1.000–0.979 Peptidase-C 3.4.-.- PEPC* 89 0.903–0.391 Proline dipeptidase 3.4.-.- PEPD-2* 56 1.000–0.798 Leucyl-L-tyrosine peptidase 3.4.-.- PEPLT* 19 1.000–0.953 Phosphogluconate dehydrogenase 1.1.1.44 PGDH* 7 1.000–0.967 Phosphoglycerate kinase 2.7.2.3 PGK-1* 14 1.000–0.930 PGK-2* 13 1.000–0.975 Phosphoglucomutase 5.4.2.2 PGM-1* 72 1.000–0.600 PGM-2* 32 1.000–0.958 Purine-nucleoside phosphorylase 2.4.2.1 PNP-1* 87 1.000–0.614 Pyruvate kinase 2.7.1.40 PK-2* 14 1.000–0.980 Triose-phosphate isomerase 5.3.1.1 TPI-1* 5 1.000–0.986 TPI-2* 0 1.000–1.000 TPI-3* 27 1.000–0.930 TPI-4* 2 1.000–0.994

ture estimates derived from 100 simulated mixtures were where PMH = the proportion of hatchery fi sh from a par- used to evaluate the accuracy of estimated contributions to ticular region in the sample of marked fi sh; each region with mixture sizes of 100, 300, and 500 fi sh. RU/RM = the ratio of unmarked to marked releases in We analyzed mixtures composed of fi sh entirely from each a region; and region and also mixtures that excluded fi sh from regions SU/SM = the ratio of unmarked to marked fi sh in our south and north of our marine sampling area. Precisions of ocean samples. the stock composition estimates for the actual mixtures were estimated by bootstrapping baseline and mixture genetic The RU/RM for 1997 and 1998 brood years varied consider-consider- data 100 times as described in Pella and Milner (1987). ably among regions: California coast 1.0, Klamath River to Stock compositions were estimated for June and Cape Blanco 0.01, Oregon coast 0.12, Columbia River 0.12, September−October. We also combined samples over sur- southern Washington coast 0.03, northern Washington veys and made separate estimates from samples of marked coast 0.69, Puget Sound 0.43, southern British Columbia (fi n-clipped and tagged hatchery fi sh) and unmarked fi sh to 0.09, and Upper Fraser River 0.80 (Lavoy1; PSMFC2). We examine hatchery and wild stock compositions. However, because not all hatchery fi sh are marked, unmarked fi sh 1 Lavoy, L. 2001. Personal commun. Washington Department are a mixture of wild and hatchery fi sh. We therefore es- of Fish and Wildlife, Olympia, WA. 98501. 2 timated the proportion of hatchery fi sh for a region in the PSMFC (Pacific States Marine Fisheries Commission). 2001. Regional Mark Information System (RMIS) coded-wire sample of unmarked fi sh (PUH) by tag on-line database. [Available from Pacifi c States Marine Fisheries Commission, 45 SE 82nd Dr., Suite 100, Gladstone, PUH = (PMH (RU/RM))/(SU/SM), (1) OR 97027-2522.] 646 Fishery Bulletin 101(3)

then subtracted PUH for each region from the genetic esti- regions, and 2.6% was due to variability among the nine mate of the region’s contribution to the sample of unmarked regions. fi sh. The sum of the remaining values estimated the pro- Genetic relationships among populations of coho salmon portion of wild fi sh in the sample of unmarked fi sh. When as revealed by two-dimensional MDS analysis showed that

PUH for a region waswas greater than the genetic estimate of genetic differences among populations were geographically the region’s contribution to the sample of unmarked fi sh, structured (Fig. 2). The fi rst axis in the plot separated pop- the percentage of wild fi sh from that region was considered ulations in coastal Oregon and California from northern to be zero. populations. Several populations, including two from the We estimated regional proportions of hatchery and wild Rogue River in southern Oregon (numbers 7 and 8) and coho salmon in the all-fi sh marine sample that included Big Qualicum hatchery (85) on Vancouver Island, were po- both marked and unmarked coho salmon. Regional hatch- sitioned near the convergence of the southern and northern ery contributions to the all-fi sh sample were made by sum- population groups. The Iron Gate hatchery sample (5) from ming each region’s estimated contribution to the sampled the Klamath River, California, clustered with the northern marked and unmarked fi sh, weighted by the proportion of population group. Several genetically discrete groups ap- each of these sample types in the total sample. Regional peared on smaller geographical scales. However, samples proportions of wild coho salmon in the all-fi sh sample from Iron Gate hatchery (5), Yaquina River (27), Nehalem were made by multiplying a region’s estimated proportion hatchery (33), Willapa Bay area (50, 51, and 52), Dungeness of wild coho salmon in the unmarked sample by the propor- hatchery (64), McGovern Creek (74), upper Cascade River tion of unmarked fi sh in the total sample. (81), and Ennis Creek (82) did not cluster with nearby populations. The single population in our study from the upper Fraser River region—Spius hatchery (89) of the Results Thompson River−was the most genetically distinct in the MDS analysis (x=−2.3, y=−0.9) and was positioned beyond Baseline genetic data and population structure the scaling shown in Figure 2. The Little River (2) popula- tion also fell outside the area of the plot (x=5.1, y=2.0), but Although coho salmon generally have low levels of genetic was genetically most similar to other California coastal variability in relation to other Pacifi c salmon, a suffi cient populations (1, 3, and 4). number of polymorphic loci were detected to distinguish many populations and regional population groups. Of 59 Genetic estimates of simulated stock mixtures loci screened in all 89 populations, 56 were polymorphic, and 29 of these were at the P0.95 level of polymorphism One demonstration of discreteness among regional groups in at least one population (Table 2). Allelic frequencies is the correct allocation in a mixed-stock analysis of simu- are reported in an appendix that can be retrieved at lated samples from baseline populations to their stock of the Northwest Fisheries Science Center website [http: origin. We used simulated sample sizes of 100, 300, and //www.nwfsc.noaa.gov]. Twenty of the 56 polymorphic loci 500 taken from one region at a time; therefore the results had two alleles per locus, 24 had three alleles per locus, represent the accuracy of reallocation back to the region of nine had four alleles, two had fi ve alleles, and one had six origin. Table 3 presents the average values of 100 bootstrap alleles. Two loci (BGALA* and PEPC*) varied in all popula- resamplings of both the baseline and the mixture samples. tions studied. Three loci (GAPDH-5*, LDH-C*, and TPI-2*) For simulated sample sizes of 100, reallocation accuracy were monomorphic in all populations. Observed genotypic ranged from 81% (coastal northern Washington) to 98% proportions for polymorphic loci in 128 samples departed (upper Fraser River population) and averaged 88.7% over signifi cantly (P<0.05) from expected Hardy-Weinberg pro- the nine regions. Average accuracy increased to 92.9% with portions in 75 of 1476 tests (5.1%). There were no consis- an increase in the size of the simulated sample to 300. Only tent trends by population or locus. Because the number of marginal improvement (93.6% accuracy) was achieved by signifi cant tests is close to the number expected by chance increasing the simulated sample size to 500. for this rejection level, we did not attach any biological We also used mixed-stock analysis of simulated samples signifi cance to these departures. to examine the accuracy of composition estimates for Cali-

The percentages of P0.95 loci and average heterozygosi- fornia, Puget Sound, and British Columbia regions when ties over 56 loci for each population appear in Table 1. The fi sh from these areas were not present in mixtures. Average percentage of P0.95 loci ranged from only 5.4% in Lewis values for sample sizes of 100 ranged from 0% (California River hatchery early run (population 41) to 17.9% in the coast, upper Fraser River) to 4% (Oregon coast) and aver- Mad River hatchery (4). Average heterozygosities ranged aged 1.8% over the fi ve regions (Table 4). Increased sample from 0.021 in Iron Gate hatchery (5) and Elk River (9) to sizes of 300 and 500 resulted in small improvements in 0.046 in Sandy River hatchery (46). Gene diversity analysis average accuracy (1.4% and 1.0 %). of the 89 populations resulted in a total gene diversity (HT) of 0.035 and an average sample diversity (HS) of 0.033. Stock compositions of ocean-caught coho salmon Thus, 94.5% of the total genetic diversity was attributable to within-sample variability and 5.5% was attributable to Genotypes for 56 loci were scored for 730 juvenile coho variability among samples. About 2.9% of the total gene salmon captured in ocean trawls in 1998−2000 (Table 5). diversity was due to variability among populations within About 65% of the 455 fi sh in June trawls were sampled Teel et al.: Genetic analysis of juvenile Oncorhynchus kisutch 647

1.2 California British Columbia 27 Yaquina R Ennis Cr McGovern Cr coast 4 upper Cascade R 84 64 Dungeness H 82 74 83 81 86 87 3 0.5 88 85 1 78 33 80 79 Nehalem H 76 73 26 12 70 75 Puget Sound 68 77 24 13 23 67 63 21 66 72 69 19 22 20 2 65 Iron Gate H 5 30 14 n 71 31 15 Oregon o 61 18 i 59 58 8 29 28 32 s north 60 62 7 coast

n 50 11 -0.2 57 10 e Washington 52 25 16 m coast i Willapa Bay H 36 38 48 D 41 43 39 9 17 40 51 34 37 46 49 6 42 44 35 45 Klamath River Columbia River 56 to Cape Blanco -0.9 55 47 south 53 Washington 54 Coast -1.6 -1.0 -0.3 0.4 1.0 1.7 Dimension 1

Figure 2 Multidimensional scaling (MDS) of Cavalli-Sforza and Edwards (1967) chord distances based on 56 allozyme loci between samples of 89 populations of coho salmon extending from northern California to southern British Columbia. Location numbers are given in Table 1 and Figure 1. Populations within regions are identifi ed with polygons where possible. Open circles indicate populations that did not cluster closely with nearby populations. Populations 2 from the California coast and 89 from the upper Fraser River fall beyond the scale of the plot.

Table 3 Mean estimated percentage contributions (± standard deviations) of 100 bootstrap resamplings of mixtures composed of fi sh from only one region. Population numbers are explained in Table 1.

n=100 n=300 n=500 Region of largest Region (populations) Estimate Estimate Estimate misallocation

California coast (1−4) 95 ±4 97 ±3 97 ±3 Oregon coast Klamath River to Cape Blanco (5−9) 94 ±5 96 ±3 96 ±3 Columbia River Oregon coast (10−33) 86 ±7 91 ±4 92 ±3 Klamath River to Cape Blanco Columbia River (34−49) 84 ±8 92 ±3 93 ±3 Oregon coast South Washington coast (50−56) 88 ±8 95 ±3 95 ±3 North Washington coast North Washington coast (57−63) 81 ±10 88 ±5 90 ±4 Puget Sound Puget Sound (64−82) 85 ±7 90 ±5 90 ±4 British Columbia British Columbia (83−88) 83 ±9 88 ±6 90 ±5 Puget Sound Upper Fraser River (89) 98 ±2 99 ±1 99 ±1 Columbia River

in the two northern most transects along the Washington caught in 1998 were too small to provide accurate mixed- coast, 24% in three transects closest to the Columbia River, stock estimates; therefore the ocean samples collected in and 10% in the four most southern transects along the 1999 and 2000, and a sample pooled over 1998−2000, were Oregon coast. Samples from these three areas comprised analyzed separately. In the 1998−2000 pooled sample, 43%, 23%, and 33%, respectively, of the 275 fi sh caught Columbia River populations were estimated to be the in September trawls. The numbers of offshore juveniles major contributing regional group in June (47%, SD=6%) 648 Fishery Bulletin 101(3)

Table 4 Actual percentage composition and mean estimated percentage contributions (± standard deviations) of 100 bootstrap resamplings of mixtures composed of 100, 300, and 500 fi sh. Population numbers are explained in Table 1.

n=100 n=300 n=500 Region (populations) Actual Estimate Estimate Estimate

California coast (1−4) 0 0 ±1 0 ±0 0 ±0 Klamath River to Cape Blanco (5−9) 0 3 ±4 2 ±2 1 ±2 Oregon coast (10−33) 20 21 ±8 20 ±5 20 ±4 Columbia River (34−49) 50 44 ±11 46 ±6 48 ±5 South Washington coast (50−56) 15 14 ±8 14 ±4 14 ±3 North Washington coast (57−63) 15 10 ±7 12 ±5 12 ±4 Puget Sound (64−82) 0 4 ±5 4 ±3 3 ±2 British Columbia (83−88) 0 2 ±3 1 ±2 1 ±1 Upper Fraser River (89) 0 0 ±1 0 ±1 0 ±0

and September (32%, SD=9%). The Oregon coastal region Discussion contributed about 18% (SD=5%) to the June mixture and 21% (SD=7%) to the September sample. The estimated con- Usefulness of coho salmon allozyme data tribution of Puget Sound fi sh to the pooled ocean samples for mixed-stock analysis was much greater in September (17%, SD=7%) than it was in June (3%, SD=2%). Although the gene diversity analysis indicated that the Genetic mixed-stock analysis of ocean-caught hatchery level of allele-frequency differentiation among populations fi sh with CWTs provided a direct comparison of genetic within regions was similar to that between regions, further estimates and a mixed-stock sample of known origins analyses showed that the magnitude of regional differen- (Brodziak et al. 1992). Only 41 fi sh had CWTs (Table 6). tiation in the baseline was suffi cient to provide accurate No fi sh with CWTs appeared in the 1998 sample. Most of mixed-stock estimates. First, we found several genetically the fi sh with CWTs in 1999 and 2000 originated from Co- discrete population groups of coho salmon over an area lumbia River (68%, n=28) and Oregon coastal (12%, n=5) extending from California to southern British Columbia. hatcheries. In the genetic analysis of the 41 fi sh, Columbia Most of the samples in the MDS plot clustered with nearby River hatcheries were estimated to contribute about 22 fi sh samples, and the north-south arrangement of neighboring (53%, SD=21%). Approximately 7 fi sh (16%, SD=17%) were population groups indicated that isolation by distance is estimated to originate from Oregon coastal hatcheries. an important component of genetic population structure Of the 730 juveniles sampled during the study, 501 on this geographic scale. As with other species of Pacifi c (69%) bore hatchery marks (clipped adipose fi ns). The per- salmon, natal homing to spawning areas is an important centage of unmarked fi sh in the September sample (35%) isolating mechanism between populations of coho salmon. was greater than that in June (29%). Genetic mixed-stock Second, the analysis of simulated stock mixtures also estimates for hatchery-marked fi sh alone indicated that demonstrated that regional differences were suffi cient to 69% (SD=6%) originated from the Columbia River and provide reliable estimates of coho salmon stock composi- 14% (SD=4%) from Oregon coastal hatcheries (Table 7). tions. Accurate estimates were obtained from simulated The sample of unmarked fi sh, which contained a mixture sample sets composed of 100% contributions from each re- of wild and unmarked hatchery fi sh, was estimated to gion (Table 3). Third, a more rigorous test of the adequacy have a much smaller proportion of Columbia River fi sh of the baseline was made by comparing genetic estimates (20%, SD=8%) but a larger proportion of coastal Oregon with direct determinations based on CWTs. These esti- (36%, SD=9%) and northern Washington (25%, SD=7%) mates were reasonably accurate, especially for the largest fi sh (Table 7). About 30% of unmarked fi sh in the pooled contributing regions (Table 6), given the small sample of ocean sample originated from hatcheries (Eq. 1) and 70% only 41 fi sh bearing CWTs. Both the simulation and CWT from wild populations. Estimated contributions from mixture results are consistent with the fi ndings of Wood et hatchery and wild populations of all ocean juveniles al. (1987) that estimation accuracy decreases substantially sampled (marked and unmarked) were 78% and 22%, re- when mixture sample sizes are small and when genetic spectively. Coho salmon originating in the Columbia River separation among stocks is limited. Lastly, the analyses were estimated to comprise 54% of the total sample, but of ocean-caught mixture samples themselves appeared to only 1% consisted of wild fi sh. Oregon coastal rivers con- provide reasonable composition estimates (Table 5). Ad- tributed 21% to the total ocean sample, and nearly equal ditionally, estimates for samples pooled over years tended proportions were contributed from hatcheries and wild to be intermediate between the two annual estimates, as populations. would be expected from pooling. Teel et al.: Genetic analysis of juvenile Oncorhynchus kisutch 649

Table 5 Estimated percentage stock compositions ( standard deviations), sample sizes (n), and recoveries of coded wire tags (CWT) for coho salmon sampled in trawl surveys along the Oregon and Washington coasts in June and September 1998, 1999, and 2000. Stock compositions were not estimated for June (n=43) and September (n=18) 1998 because of small sample sizes. None of the 1998 samples contained coded wire tags.

June September

Region Est. CWT Est. CWT

1999 n 278 152 California coast 0 ±1 0 0 ±0 0 Klamath River to Cape Blanco 6 ±6 0 0 ±0 0 Oregon coast 25 ±7 5 25 ±8 0 Columbia River 46 ±9 8 20 ±14 4 South Washington coast 11 ±4 2 9 ±5 0 North Washington coast 10 ±5 2 18 ±15 0 Puget Sound 3 ±4 0 25 ±9 1 British Columbia 0 ±1 0 3 ±3 0 Upper Fraser River 0 ±0 0 0 ±0 0 2000 n 134 105 California coast 0 ±0 0 1 ±3 0 Klamath River to Cape Blanco 1 ±7 0 0 ±0 0 Oregon coast 11 ±7 0 17 ±8 0 Columbia River 40 ±11 11 48 ±16 5 South Washington coast 17 ±7 0 6 ±9 0 North Washington coast 21 ±11 0 10 ±16 0 Puget Sound 11 ±8 0 14 ±7 1 British Columbia 0 ±0 0 3 ±8 2 Upper Fraser River 0 ±0 0 0 ±0 0 1998, 1999, and 2000 combined n 455 275 California coast 0 ±0 0 0 ±0 0 Klamath River to Cape Blanco 7 ±4 0 0 ±0 0 Oregon coast 18 ±5 5 21 ±7 0 Columbia River 47 ±6 19 32 ±9 9 South Washington coast 11 ±3 2 9 ±4 0 North Washington coast 13 ±4 2 19 ±11 0 Puget Sound 3 ±2 0 17 ±7 2 British Columbia 0 ±0 0 2 ±2 2 Upper Fraser River 0 ±0 0 0 ±0 0

Nonetheless, the usefulness of the allozyme baseline that will likely be based on DNA variability because coho salmon we compiled for coho salmon is limited by two factors. First, minisatellite (Miller et al., 1996; Beacham et al., 1996) and few samples in the baseline are from California and British microsatellite (Small et al., 1998a; 1998b; Beacham et al., Columbia populations. Although the baseline appears to be 2001) loci show much higher levels of polymorphism than adequate to analyze stock mixtures of juvenile coho salmon do allozyme loci. Recently, variation at eight microsatellite off Oregon and Washington, mixed stock analyses of sam- DNA loci and one Mhc locus in coho salmon populations ples from other marine areas, particularly to the north, re- in British Columbia and Washington was used to estimate quires the sampling of additional populations. Second, our the stock compositions of fi sheries off the west coast of study demonstrated that estimates of stock compositions Vancouver Island (Shaklee et al., 1999; Beacham et al., are not suffi ciently accurate to effectively identify stock 2001). However, the use of highly polymorphic microsatel- groups that are absent from mixtures or present in small lite loci may not provide increased discrimination among proportions (Tables 4 and 6). Estimation accuracy can be populations on large geographical scales because of allelic improved by using additional gene markers. These markers convergence from multiple mutations (Nauta and Weiss- 650 Fishery Bulletin 101(3)

ing, 1996). Nonetheless, the extension of a DNA baseline to tagged juvenile coho salmon and concluded they were not include populations in Oregon and California, may resolve highly migratory, often remaining close to their point of sea fi ne-scale (geographic and temporal) differences between entry for several months. Our genetic results corroborate coho salmon populations in southern coastal areas. that fi nding. Genetic estimates indicate that about 89% of ocean juveniles caught in June and 81% in September Stock compositions of ocean-caught juvenile originated from the Columbia River and adjacent coastal coho salmon rivers. Recoveries of hatchery-tagged fi sh (n=41) also indi- cate that juveniles remain near river mouths in their fi rst Studies using large purse seines conducted in 1981−85 few months after ocean entry; only three of these CWT- revealed that juvenile coho salmon were the most abundant marked fi sh came from hatcheries in other regions. of the Oncorhynchus species in the nearshore areas along However, our genetic results indicate that a change has the Oregon and Washington coasts (Pearcy and Fisher, 1988; occurred in the distribution of Washington coastal and 1990). Pearcy and Fisher (1988; 1990) captured hatchery- Puget Sound juvenile coho salmon. In the 1980s, juvenile coho salmon from Washington coastal hatcheries were not recovered along the Washington and Oregon coasts after mid summer, apparently having migrated northward Table 6 (Pearcy and Fisher, 1988). Pearcy and Fisher (1990) also Actual composition and estimated contributions (± stan- found that Puget Sound coho salmon did not migrate along dard deviations) of a mixture of 41-CWT fi sh. the Washington and Oregon coast until sometime between their fi rst and second summer at sea. However, our genetic Actual Genetic estimate results showed that in 1998−2000 fi sh from Washington Region Number % Number % coastal streams and hatcheries comprised substantial proportions of the juveniles in nearshore areas along California coast 0 0 1 3 ±4 the Washington and Oregon coast in both early and late Klamath River to summer (24% and 28%). We also found that juvenile coho Cape Blanco 0 0 0 0 ±0 salmon from Puget Sound are present in late summer. Our Oregon coast 5 12 7 16 ±17 fi nding that coho salmon from northern stocks move south Columbia River 28 68 22 53 ±21 along the coast during their fi rst summer was substanti- South Washington coast 2 5 0 0 ±0 ated by the catch of CWT-marked fi sh originating from North Washington coast 3 7 5 11 ±9 Puget Sound (n=2) and southern British Columbia (n=2). Puget Sound 1 2 5 11 ±18 Recent reductions in the number of coho salmon smolts British Columbia 2 5 2 6 ±11 released from the region’s hatcheries have not resulted in Upper Fraser River 0 0 0 0 ±0 a decrease in the proportion of hatchery juveniles along the Oregon and Washington coasts. Annual releases of hatch-

Table 7 Estimated percentage stock compositions and sample sizes for populations of marked (fi sh with clipped adipose fi ns) and unmarked coho salmon sampled in trawl surveys along the Oregon and Washington coasts in 1998, 1999, and 2000. Samples from June and September were combined. Separate estimates for the contributions of hatchery and wild stocks were made by using estimates of hatchery marking rates for each region.

Marked fi sh Unmarked fi sh (hatchery fi sh) (hatchery and Wild fi sh) All fi sh Genetic estimate Genetic estimate (n=501) (n=229) Hatchery Wild Hatchery Wild Total Region (%) (%) (%) (%) (%) (%) (%)

California coast 0 ±0 1 ±2 0 1 0 0 0 Klamath River to Cape Blanco 1 ±2 1 ±7 0 1 1 0 1 Oregon coast 14 ±4 36 ±9 4 32 11 10 21 Columbia River 69 ±6 20 ±8 18 2 53 1 54 South Washington coast 4 ±4 9 ±5 0 9 3 3 6 North Washington coast 1 ±7 25 ±7 2 23 1 7 8 Puget Sound 6 ±5 8 ±5 6 2 6 1 7 British Columbia 5 ±2 0 ±0 0 0 3 0 3 Upper Fraser River 0 ±0 0 ±0 0 0 0 0 0 Total 100 100 30 70 78 22 100 Teel et al.: Genetic analysis of juvenile Oncorhynchus kisutch 651

ery smolts exceeded 64 million fi sh during the early 1980s Beacham, T. D., K. M. Miller, and R. E. Withler. but have decreased to about 39 million in recent years, a 1996. Minisatellite DNA variation and stock identifi cation 40% reduction (PSMFC2; NRC3). Nonetheless, the propor- of coho salmon. J. Fish Biol. 49:411−429. tion of hatchery coho salmon in nearshore marine waters Beamish, R. J., D. McCaughran, J. R. King, R. M. Sweeting, and G. A. McFarlane. has remained high, averaging 74% in 1981−85 (Pearcy and 2000. Estimating the abundance of juvenile coho salmon in Fisher, 1990) and 78% in 1998−2000 (present study). This the Strait of Georgia by means of surface trawls. North result, therefore, leads to the conclusion that the number Am. J. Fish. Manage. 20:369−375. of naturally produced juveniles in Oregon and Washington Brodziak, J., B. Bentley, D. Bartley, G.A.E. Gall, R. Gomulkiewicz, coastal waters has also decreased proportionately during and M. Mangel. this period. If so, wild populations of coho salmon may also 1992. Tests of genetic stock identifi cation using coded wire have experienced a decline in abundance on the order of tagged fi sh. Can. J. Fish. Aquat. Sci. 49:1507−1517. 40%. Cavalli-Sforza, L. L., and A. W. F. Edwards. Steep declines in Columbia River wild populations are 1967. Phylogenetic analysis: models and estimation pro- particularly evident. At the beginning of the 20th century, cedures. Evolution 21:550−570. Chakraborty, R., M. Hagg, N. Ryman, and G. Stahl. populations in the Columbia River are thought to have 1982. Hierarchical gene diversity analysis and its applica- been the largest producers of coho salmon in the region tion to brown trout population data. Hereditas 97:17−21. (Chapman, 1986; Lichatowich, 1989) and likely contributed Chapman, D. W. a substantial proportion to the nearshore population of ju- 1986. Salmon and steelhead abundance in the Columbia venile salmon. At present, Columbia River juveniles pre- River in the nineteenth century. Trans. Am. Fish. Soc. dominate along the coast. However, these fi sh are almost 115:662−670. entirely releases from hatchery facilities and Columbia Debevec, E. M., R. B. Gates, M. Masuda, J. Pella, J. Reynolds, and River wild coho salmon are conspicuously absent. L. W. Seeb. 2000. SPAM (version 3.2): statistics program for analyzing mixtures. J. Hered. 91:509−511. Acknowledgments Emmett, R. L., and R. D. Brodeur. 2000. Recent changes in the pelagic nekton community off Oregon and Washington in relation to some physical oceano- We are grateful to George Milner and Paul Aebersold who graphic conditions. North Pacifi c Anadr. Fish Comm. Bull. developed much of the allozyme baseline for coho salmon. 2:11−20. Sewall Young, Laurie Weitkamp, Kathleen Neely, Bill Godfrey, H. Waknitz, Kathryn Kostow, Orlay Johnson, Ken Currens, 1965. Coho salmon in offshore waters. In Salmon of the Eric Beamer, Scott Chitwood, Doug Cramer, Marc Miller, North Pacifi c Ocean. Part IX. Coho, chinook, and masu and Jennifer Nielsen provided baseline samples. We thank salmon in offshore waters, p. 1–39. Int. North Pacific Ed Casillas, Ric Brodeur, Bob Emmett, Cindy Bucher, Susan Fish. Comm. Bull. 16. Hinton, Cheryl Morgan, Paul Bentley, and Joe Fisher for Guo, S. W., and E. A. Thompson. 1992. Performing the exact test of Hardy-Weinberg propor- providing coho salmon samples and data from their coastal tions for multiple alleles. Biometrics 48:361−372. salmon surveys. This study was supported in part by funds Guthrie, C. M., E. V. Farley Jr., N. M. L. Weemes, and from the Bonneville Power Administration and the U.S. E. C. Martinson. GLOBEC program as part of an initiative to understand 2000. Genetic stock identifi cation of sockeye salmon cap- the effects of ocean dynamics on salmon populations. tured in the coastal waters of Unalaska island during April/May and August 1998. North Pacifi c Anadr. Fish Comm. Bull. 2:309−315. Literature cited Hartt, A. C., and M. B. Dell. 1986. Early oceanic migrations and growth of juvenile Aebersold, P. B., G. A. Winans, D. J. Teel, G. B. Milner, and Pacific salmon and steelhead trout. Int. N. Pac. Fish. F. M. Utter. Comm. Rep. 46, 105 p. 1987. Manual for starch gel electrophoresis: a method for the Johnson, O. W., T. A. Flagg, D. J. Maynard, G. B. Milner, and detection of genetic variation. U.S. Dep. Commer., NOAA F. W. Waknitz. Tech. Report NMFS 61, 19 p. 1991. Status review for lower Columbia River coho salmon. Beacham, T. D., J. R. Candy, K. J. Supernault, T. Ming, B. Deale, U.S. Dep. Commerce, NOAA Tech. Memo. NMFS F/NWC- A. Schulze, D. Tuck, K. H. Kaukauna, J. R. Irvine, K. M. Miller, 202, 94 p. and R. E. Wither. Lawson, P. W., and R. M. Comstock. 2001. Evaluation and application of microsatellite and major 2000. The proportional migration selective fi shery model. histocompatibility complex variation for stock identifi cation In Sustainable fi sheries management: Pacifi c salmon (E. E. of coho salmon in British Columbia. Trans. Am. Fish. Soc. Knudsen, C. R. Steward, D. D. MacDonald, J. E. Williams, 130:1116−1149. and D. W. Reiser, eds.), p. 423−433. Lewis Publishers, Boca Raton, FL. Lichatowich, J. A. 1989. Habitat alteration and changes in abundance of coho 3 NRC (Natural Resource Consultants, Inc.). 1995. Database (Oncorhynchus kisutch) and chinook (Oncorhynchus tshaw- of artificially propagated anadromous salmon (database). ytscha) salmon in Oregon’s coastal streams. In Proceed- [Available from Environmental and Technical Services Division, ings of the national workshop on effects of habitat alteration NMFS, 525 N.E., Oregon Street, Portland, OR 97232.] on salmonid stocks, May 6−8, 1987, Nanaimo, B.C. (C. D. 652 Fishery Bulletin 101(3)

Levings, L. B. Holtby, and M. A. Henderson, eds.), p. 92−99. Shaklee, J. B., T. D. Beacham, L. Seeb, and B. A. White. Can. Spec. Publ. Fish. Aquat. Sci. 105. 1999. Managing fi sheries using genetic data: case studies Miller, K. M., R. E. Withler, and T. D. Beacham. from four species of Pacifi c Salmon. Fish. Res. 43:45−78. 1996. Stock identifi cation of coho salmon (Oncorhynchus Small, M. P., R. E. Withler, and T. D. Beacham. kisutch) using minisatellite DNA variation. Can. J. Fish. 1998a. Population structure and stock identifi cation of Brit- Aquat. Sci. 53:181−195. ish Columbia coho salmon (Oncorhynchus kisutch) based on Milner, G. B., D. J. Teel, F. M. Utter, and G. A. Winans. microsatellite DNA variation. Fish. Bull. 96:843−858. 1985. A genetic method of stock identifi cation in mixed Small, M. P., T. D. Beacham, R. E. Withler, and R. J. Nelson. populations of Pacifi c salmon, Oncorhynchus spp. Mar. 1998b. Discriminating coho salmon (Oncorhynchus kisutch) Fish. Rev. 47:1−8. populations within the Fraser River, British Columbia, Nauta, M. J., and F. J. Weissing. using microsatellite DNA markers. Mol. Ecol. 7:141−155. 1996. Constraints on allele size at microsatellite loci: implica- Swofford, D. L., and R. B. Selander. tions for genetic differentiation. Genetics. 143:1021−1032. 1981. BIOSYS-1: a FORTRAN program for the comprehen- Nei, M. sive analysis of electrophoretic data in population genetics 1978. Estimation of average heterozygosity and genetic and systematics. J. Hered. 72:281−283. distance from a small number of individuals. Genetics Utter, F., P. Aebersold, and G. Winans. 89:583−590. 1987. Interpreting genetic variation detected by electro- Orsi, J. A., M. V. Sturdevant, J. M. Murphy, D. G. Mortensen, and phoresis. In Population genetics and fi shery management B. L. Wing. (N. Ryman and F. Utter, eds.), p. 21–45. Washington Sea 2000. Seasonal habitat use and early marine ecology of juve- Grant, Univ. Washington Press, Seattle, WA. nile Pacifi c salmon in southeastern Alaska. North Pacifi c Van Doornik, D. M., M. J. Ford, and D. J. Teel. Anadr. Fish Comm. Bull. 2:111−122. 2002. Patterns of temporal genetic variation in coho sal- Pearcy, W. G., and J. P. Fisher. mon: estimates of the effective proportion of 2-year-olds in 1988. Migrations of coho salmon, Oncorhynchus kisutch, natural and hatchery populations. Trans. Am. Fish. Soc. during their first summer in the ocean. Fish. Bull. 86: 131:1007−1019. 173−195. Waples, R. S. 1990. Distribution and abundance of juvenile salmonids off 1988. Estimation of allele frequencies at isoloci. Genetics Oregon and Washington, 1981−1985. U.S. Dep. Commerce, 118:371−384. NOAA Tech. Report NMFS 93, 83 p. 1990. Temporal changes of allele frequencies in Pacific Pella, J., and G. B. Milner. salmon: implications for mixed-stock fi shery analysis. Can. 1987. Use of genetic marks in stock composition analyses. J. Fish. Aquat. Sci. 47:968−976. In Population genetics and fi shery management (N. Ryman Weitkamp, L. A., T. C. Wainright, G. J. Bryant, G. B. Milner, and F. Utter, eds.), p. 247−276. Washington Sea Grant, D. J. Teel, T. G. Kope, and R. S. Waples. Univ. Washington Press, Seattle, WA. 1995. Status review of coho salmon from Washington, Ore- Raymond, M., and F. Rousset. gon, and California. U.S. Dep. Commer., NOAA Tech. 1995. GENEPOP (versions 1.2 and 3.1): population genet- Memo. NMFS-NWFSC-24, 258 p. ics software for exact tests and ecumenism. Heredity 86: Wood, C. C., S. McKinnell, T. J. Mulligan, and D. A. Fournier. 248−249. 1987. Stock Identifi cation with the maximum likelihood Shaklee, J. B., F. W. Allendorf, D. C. Morizot, and G. S. Whitt. mixture model: sensitivity analysis and application to com- 1990. Gene nomenclature for protein-coding loci in fi sh. plex problems. Can. J. Fish. Aquat. Sci. 44:866−881. Trans. Am. Fish. Soc. 119:2−15.